Homeostatic Disinhibition in the aging brain and alzheimer's disease

Journal of Alzheimer's Disease

Volumn 24, Issue 1, 2011, Pages 15-24

  Gleichmann, Marc ^a   Chow, Vivian W ^b   Mattson, Mark P ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alzheimer's disease; cognitive reserve; disinhibition; GABA; interneuron; neuronal activity

Indexed keywords

3 AMINOPROPYLBUTYLPHOSPHINIC ACID; 4 AMINOBUTYRIC ACID B RECEPTOR BLOCKING AGENT; ACTIVATION INDUCED CYTIDINE DEAMINASE; ALPHA ADRENERGIC RECEPTOR BLOCKING AGENT; AMYLOID; AMYLOID PRECURSOR PROTEIN; BRAIN DERIVED NEUROTROPHIC FACTOR; CANNABINOID RECEPTOR ANTAGONIST; MEMANTINE; METABOTROPIC RECEPTOR; METABOTROPIC RECEPTOR ANTAGONIST; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR STIMULATING AGENT;

AGING; ALLOSTERISM; ALZHEIMER DISEASE; ARTICLE; BEHAVIOR THERAPY; BRAIN NERVE CELL; ELECTROSTIMULATION THERAPY; EPILEPSY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GABAERGIC TRANSMISSION; GAMMA RHYTHM; GLUTAMATERGIC TRANSMISSION; HALLUCINATION; HOMEOSTASIS; HOMEOSTATIC DISHINHIBITION; HUMAN; LONG TERM POTENTIATION; MILD COGNITIVE IMPAIRMENT; NERVE CELL PLASTICITY; NEUROTRANSMISSION; PRIORITY JOURNAL; RISK FACTOR; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; TRANSCRANIAL DIRECT CURRENT STIMULATION; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 79955662632     PISSN: 13872877     EISSN: None     Source Type: Journal    
DOI: 10.3233/JAD-2010-101674     Document Type: Article

References (85)

1. Citron M (2010) Alzheimer's disease: strategies for disease modification. Nat Rev Drug Discov 9, 387-398.
2. Creed MC, Milgram NW (2008) Amyloid-modifying ther-apies for Alzheimer's disease: therapeutic progress and its implications. Age (Dordr) 32, 365-384.
3. Reiman EM, Langbaum JB, Tariot PN (2010) Alzheimer's prevention initiative: a proposal to evaluate presymptomatic treatments as quickly as possible. Biomark Med 4, 3-14.
4. Khachaturian ZS (2010) Perspective on the Alzheimer's dis-ease neuroimaging initiative: progress report and future plans. Alzheimers Dement 6, 199-201.
5. Beckett LA, Harvey DJ, Gamst A, Donohue M, Kornak J, Zhang H, Kuo JH; Alzheimer's Disease Neuroimaging Initiative (2010) The alzheimer's disease neuroimaging ini-tiative: annual change in biomarkers and clinical outcomes. Alzheimers Dement 6, 257-264.
6. Weiner MW, Aisen PS, Jack CR Jr, Jagust WJ, Trojanowski JQ, Shaw L, Saykin AJ, Morris JC, Cairns N, Beckett LA, Toga A, Green R, Walter S, Soares H, Snyder P, Siemers E, Potter W, Cole PE, Schmidt M; Alzheimer's Disease Neuroimaging Initiative (2010) The Alzheimer's disease neuroimaging initiative: progress report and future plans. Alzheimers Dement 6, 202-211.
7. Fagan AM, Holtzman DM (2010) Cerebrospinal fluid bio-markers of Alzheimer's disease. Biomarker Med 4, 51-63.
8. Snowdon DA; Nun Study (2003) Healthy aging and dementia: findings from the Nun Study. Ann Intern Med 139, 450-454. (Pubitemid 38120875)
9. Braak H, Braak E (1995) Staging of Alzheimer's disease-related neurofibrillary changes. Neurobiol Aging 16, 271-278.
10. Nelson PT, Braak H, Markesbery WR (2009) Neuropathology and cognitive impairment in Alzheimer disease: a complex but coherent relationship. J Neuropathol Exp Neurol 68, 1-14.
11. Kashon ML, Ross GW, O'Callaghan JP, Miller DB, Petrovitch H, Burchfiel CM, Sharp DS, Markesbery WR, Davis DG, Hardman J, Nelson J, White LR (2004) Associa-tions of cortical astrogliosis with cognitive performance and dementia status. J Alzheimers Dis 6, 595-604. (Pubitemid 40164166)
12. McGeer PL, Kawamata T, Walker DG, Akiyama H, Tooyama I, McGeer EG (1993) Microglia in degenerative neurological disease. Glia 7, 84-92.
13. McGeer EG, McGeer PL (2010) Neuroinflammation in Alzheimer's disease and mild cognitive impairment: a field in its infancy. J Alzheimers Dis 19, 355-361.
14. Whitehouse PJ, Price DL, Struble RG, Clark AW, Coyle JT, Delon MR (1982) Alzheimer's disease and senile dementia: loss of neurons in the basal forebrain. Science 215, 1237-1239. (Pubitemid 12106486)
15. Samuels ER, Szabadi E (2010) Functional neuroanatomy of the noradrenergic locus coeruleus: its roles in the regulation of arousal and autonomic function. Part II: physiological and pharmacological manipulations and pathological alterations oflocus coeruleus activityinhumans. Curr Neuropharmacol 6, 254-285.
16. Simic G, Stanic G, Mladinov M, Jovanov-Milosevic N, Kostovic I, Hof PR (2009) Does Alzheimer's disease begin in the brainstem? Neuropathol Appl Neurobiol 35, 532-554.
17. Davies P, Katzman R, Terry RD (1980) Reduced somatostatin-like immunoreactivity in cerebral cortex from cases of Alzheimer disease and Alzheimer senile dementa. Nature 288, 279-280. (Pubitemid 11165878)
18. Davies CA, Mann DM, Sumpter PQ, Yates PO (1987) A quan-titative morphometric analysis of the neuronal and synaptic content of the frontal and temporal cortex in patients with Alzheimer's disease. J Neurol Sci 78, 151-164. (Pubitemid 17031709)
19. Davies P, Anderton B, Kirsch J, Konnerth A, Nitsch R, Sheetz M (1998) First one in, last one out: the role of gabaergic transmission in generation and degeneration. Prog Neurobiol 55, 651-658. (Pubitemid 28293586)
20. Masliah E, Honer WG, Mallory M, Voigt M, Kushner P, Hansen L, Terry R (1994) Topographical distribution of synaptic-associated proteins in the neuritic plaques of Alzheimer's disease hippocampus. Acta Neuropathol 87, 135-142.
21. Howlett DR, Richardson JC (2009) The pathology of APP transgenic mice: a model of Alzheimer's disease or simply overexpression of APP? Histol Histopathol 24, 83-100.
22. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, Kayed R, Metherate R, Mattson MP, Akbari Y, LaFerla FM (2003) Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunc-tion. Neuron 39, 409-421. (Pubitemid 36937044)
23. Loerch PM, Lu T, Dakin KA, Vann JM, Isaacs A, Geula C, Wang J, Pan Y, Gabuzda DH, Li C, Prolla TA, Yankner BA (2008) Evolution of the aging brain transcriptome and synaptic regulation. PLoS One 3, e3329.
24. Hendry SH, Jones EG (1988) Activity-dependent regulation of GABA expression in the visual cortex of adult monkeys. Neuron 1, 701-712.
25. Benson DL, Huntsman MM, Jones EG (1994) Activity-dependent changes in GAD and preprotachykinin mRNAs in visual cortex of adult monkeys. Cereb Cortex 4, 40-51. (Pubitemid 24066071)
26. Tallent MK (2007) Somatostatin in the dentate gyrus. Prog Brain Res 163, 265-284. (Pubitemid 47321440)
27. de Lima AD, Opitz T, Voigt T (2004) Irreversible loss of a subpopulation of cortical interneurons in the absence of glu-tamatergic network activity. Eur J Neurosci 19, 2931-2943. (Pubitemid 38822583)
28. Zhang X, Odom DT, Koo SH, Conkright MD, Canettieri G, Best J, Chen H, Jenner R, Herbolsheimer E, Jacobsen E, Kadam S, Ecker JR, Emerson B, Hogenesch JB, Unterman T, Young RA, Montminy M (2005) Genome-wide analysis of cAMP-response element binding protein occupancy, phos-phorylation, and target gene activation in human tissues. Proc Natl Acad Sci US A 102, 4459-4464. (Pubitemid 40397134)
29. Braun I, Genius J, Grunze H, Bender A, Möller HJ, Rujescu D (2007) Alterations of hippocampal and prefrontal GABAer-gic interneurons in an animal model of psychosis induced by NMDA receptor antagonism. Schizophr Res 97, 254-263. (Pubitemid 350088379)
30. Gleichmann M, Zhang Y, Wood WH, Becker KG, Mughal MR, Pazin MJ, van Praag H, Kobilo T, Zonderman AB, Troncoso JC, Markesbery WR, Mattson MP (2010) Molecular changes in brain aging and Alzheimer's disease are mirrored in experimentally silenced cortical neuron networks. Neuro-biol Dis (2010 Oct 12) [Epub ahead of print].
31. Lu T, Pan Y, Kao SY, Li C, Kohane I, Chan J, Yankner BA (2004) Gene regulation and DNA damage in the ageing human brain. Nature 429, 883-891. (Pubitemid 38843301)
32. Blalock EM, Geddes JW, Chen KC, Porter NM, Markesbery WR, Landfield PW (2004) Incipient Alzheimer's disease: microarray correlation analyses reveal major transcriptional and tumor suppressor responses. Proc Natl Acad Sci USA 101, 2173-2178. (Pubitemid 38229034)
33. Tan MG, Chua WT, Esiri MM, Smith AD, Vinters HV, Lai MK (2010) Genome wide profiling of altered gene expression in the neocortex of Alzheimer's disease. J Neurosci Res 88, 1157-1169.
34. Fraser HB, Khaitovich P, Plotkin JB, Pääbo S, Eisen MB (2005) Aging and gene expression in the primate brain. PLoS Biol 3, e274.
35. Satoh J, Tabunoki H, Arima K (2009) Molecular network analysis suggests aberrant CREB-mediated gene regulation in the Alzheimer disease hippocampus. Dis Markers 27, 239-252.
36. Corrada MM, Brookmeyer R, Paganini-Hill A, Berlau D, Kawas CH (2010) Dementia incidence continues to increase with age in the oldest old: the 90+ study. Ann Neurol 67, 114-121.
37. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, Smith I, Brett FM, Farrell MA, Rowan MJ, Lemere CA, Regan CM, Walsh DM, Sabatini BL, Selkoe DJ (2008) Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 14, 837-842.
38. Laurén J, Gimbel DA, Nygaard HB, Gilbert JW, Strittmatter SM (2009) Cellular prion protein mediates impairment of synaptic plasticity by amyloid-beta oligomers. Nature 457, 1128-1132.
39. Nimmrich V, Grimm C, Draguhn A, Barghorn S, Lehmann A, Schoemaker H, Hillen H, Gross G, Ebert U, Bruehl C (2008) Amyloid beta oligomers (A beta(1-42) globulomer) suppress spontaneous synaptic activity by inhibition of P/Q-type calcium currents. J Neurosci 28, 788-797. (Pubitemid 351159014)
40. Hillen H, Barghorn S, Striebinger A, Labkovsky B, Müller R, Nimmrich V, Nolte MW, Perez-Cruz C, van der Auwera I, van Leuven F, van Gaalen M, Bespalov AY, Schoemaker H, Sullivan JP, Ebert U (2010) Generation and therapeutic efficacy of highly oligomer-specific beta-amyloid antibodies. J Neurosci30, 10369-10379.
41. Ondrejcak T, Klyubin I, Hu NW, Barry AE, Cullen WK, Rowan MJ (2010) Alzheimer's disease amyloid beta-protein and synaptic function. Neuromolecular Med 12, 13-26.
42. Boric K, Muñoz P, Gallagher M, Kirkwood A (2008) Potential adaptive function for altered long-term potentiation mecha-nisms in aging hippocampus. J Neurosci 28, 8034-8039.
43. Minkeviciene R, Rheims S, Dobszay MB, Zilberter M, Hartikainen J, Fülöp L, Penke B, Zilberter Y, Harkany T, Pitkänen A, Tanila H (2009) Amyloid beta-induced neuronal hyperexcitability triggers progressive epilepsy. JNeurosci 29, 3453-3462.
44. Palop JJ, Mucke L (2010) Amyloid-beta-induced neuronal dysfunction in Alzheimer's disease: from synapses toward neural networks. Nat Neurosci 13, 812-818.
45. Larner AJ (2010) Epileptic seizures in AD patients. Neuro¬molecular Med 12, 71-77.
46. Palop JJ, Mucke L (2010) Synaptic depression and aberrant excitatory network activity in Alzheimer's disease: two faces of the same coin? Neuromolecular Med 12, 48-55.
47. Bishop NA, Lu T, Yankner BA (2010) Neural mechanisms of ageing and cognitive decline. Nature 464, 529-535.
48. Cheung KH, Mei L, Mak DO, Hayashi I, Iwatsubo T, Kang DE, Foskett JK (2010) Gain-of-function enhancement of IP3 receptor modal gating by familial Alzheimer's disease-linked presenilin mutants in human cells and mouse neurons. Sci Signal 3, ra22.
49. Gleichmann M, Mattson M (2010) Neuronal calcium home-ostasis and dysregulation. Antioxid Redox Signal, in press.
50. Bezprozvanny I, Mattson MP (2008) Neuronal calcium mis-handling and the pathogenesis of Alzheimer's disease. Trends Neurosci 31, 454-463.
51. Herrmann CS, Demiralp T (2005) Human EEG gammaoscil-lations in neuropsychiatric disorders. Clin Neurophysiol 116, 2719-2733. (Pubitemid 41714021)
52. Jagust WJ, Bandy D, Chen K, Foster NL, Landau SM, Mathis CA, Price JC, Reiman EM, Skovronsky D, Koeppe RA; Alzheimer's Disease Neuroimaging Initiative (2010) The Alzheimer's disease neuroimaging initiative positron emis-sion tomography core. Alzheimers Dement 6, 221-229.
53. Sperling RA, Dickerson BC, Pihlajamaki M, Vannini P, LaViolette PS, Vitolo OV, Hedden T, Becker JA, Rentz DM, Selkoe DJ, Johnson KA (2010) Functional alterations in mem-ory networks in early Alzheimer's disease. Neuromolecular Med 12, 27-43.
54. Park DC, Reuter-Lorenz P (2009) The adaptive brain: aging and neurocognitive scaffolding. Annu Rev Psychol 60, 173-196.
55. Sperling RA, Laviolette PS, O'Keefe K, O'Brien J, Rentz DM, Pihlajamaki M, Marshall G, Hyman BT, Selkoe DJ, Hedden T, Buckner RL, Becker JA, Johnson KA (2009) Amyloid deposition is associated with impaired default net-work function in older persons without dementia. Neuron 63, 178-188.
56. Northoff G, Walter M, Schulte RF, Beck J, Dydak U, Henning A, Boeker H, Grimm S, Boesiger P (2007) GABA concentra-tions in the human anterior cingulate cortex predict negative BOLD responses in fMRI. Nat Neurosci 10, 1515-1517. (Pubitemid 350175872)
57. Donahue MJ, Near J, Blicher JU, Jezzard P (2010) Baseline GABA concentration and fMRI response. Neuroimage 53, 392-398.
58. Muthukumaraswamy SD, Edden RA, Jones DK, Swettenham JB, Singh KD (2009) Resting GABA concentration predicts peak gamma frequency and fMRI amplitude in response to visual stimulation in humans. Proc Natl Acad Sci USA 106, 8356-8361.
59. O'Brien JL, O'Keefe KM, LaViolette PS, DeLuca AN, Blacker D, Dickerson BC, Sperling RA (2010) Longitudinal fMRI in elderly reveals loss of hippocampal activation with clinical decline. Neurology 74, 1969-1976.
60. Mattson MP (2008) Glutamate and neurotrophic factors in neuronal plasticity and disease. Ann N Y Acad Sci 1144, 97-112.
61. Rex CS, Lauterborn JC, Lin CY, Kramár EA, Rogers GA, Gall CM, Lynch G (2006) Restoration of long-term potentiation in middle-aged hippocampus after induction of brain-derived neurotrophic factor. J Neurophysiol 96, 677-685. (Pubitemid 44155208)
62. Stranahan AM, Lee K, Martin B, Maudsley S, Golden E, Cutler RG, Mattson MP (2009) Voluntary exercise and caloric restriction enhance hippocampal dendritic spine den-sity and BDNF levels in diabetic mice. Hippocampus 19, 951-961.
63. Li G, Peskind ER, Millard SP, Chi P, Sokal I, Yu CE, Bekris LM, Raskind MA, Galasko DR, Montine TJ (2009) Cere-brospinal fluid concentration of brain-derived neurotrophic factor and cognitive function in non-demented subjects. PLoS One 4, e 5424.
64. Phillips HS, Hains JM, Armanini M, Laramee GR, John-son SA, Winslow JW (1991) BDNF mRNA is decreased in the hippocampus of individuals with Alzheimer's disease. Neuron 7, 695-702.
65. Peng S, Garzon DJ, Marchese M, Klein W, Ginsberg SD, Francis BM, Mount HT, Mufson EJ, Salehi A, Fahnestock M (2009) Decreased brain-derived neurotrophic factor depends on amyloid aggregation state in transgenic mouse models of Alzheimer's disease. J Neurosci 29, 9321-9329.
66. Blurton-Jones M, Kitazawa M, Martinez-Coria H, Castello NA, Müller FJ, Loring JF, Yamasaki TR, Poon WW, Green KN, LaFerla FM (2009) Neural stem cells improve cognition via BDNF in a transgenic model of Alzheimer disease. Proc Natl Acad Sci USA 106, 13594-13599.
67. Nagahara AH, Merrill DA, Coppola G, Tsukada S, Schroeder BE, Shaked GM, Wang L, Blesch A, Kim A, Conner JM, Rockenstein E, Chao MV, Koo EH, Geschwind D, Masliah E, Chiba AA, Tuszynski MH (2009) Neuroprotec-tive effects of brain-derived neurotrophic factor in rodent and primate models of Alzheimer's disease. Nat Med 15, 331-337.
68. Lisman JE, Coyle JT, Green RW, Javitt DC, Benes FM, Heckers S, Grace AA (2008) Circuit-based framework for understanding neurotransmitter and risk gene interactions in schizophrenia. Trends Neurosci 31, 234-242.
69. Froestl W, Gallagher M, Jenkins H, Madrid A, Melcher T, Teichman S, Mondadori CG, Pearlman R (2004) SGS742: the first GABA(B) receptor antagonist in clinical trials. Biochem Pharmacol 68, 1479-1487. (Pubitemid 39286451)
70. Ridha BH, Josephs KA, Rossor MN (2005) Delusions and hallucinations indementia withLewy bodies: worsening with memantine. Neurology 65, 481-482. (Pubitemid 41099820)
71. Monastero R, Camarda C, Pipia C, Camarda R (2007) Visual hallucinations and agitation in Alzheimer's disease due to memantine: report of three cases. J Neurol Neurosurg Psy-chiatry 78, 546. (Pubitemid 46662914)
72. Lipton SA (2006) Paradigm shift in neuroprotection by NMDA receptor blockade: memantine and beyond. Nat Rev Drug Discov 5, 5160-5170.
73. Penner MR, Roth TL, Barnes CA, Sweatt JD (2010) An epige-netic hypothesis of aging-related cognitive dysfunction. Front Aging Neurosci 2, 9.
74. Owen AM, Hampshire A, Grahn JA, Stenton R, Dajani S, Burns AS, Howard RJ, Ballard CG (2010) Putting brain train-ing to the test. Nature 465, 775-778.
75. Basak C, Boot WR, Voss MW, Kramer AF (2008) Can training in a real-time strategy video game attenuate cognitive decline in older adults? Psychol Aging 23, 765-777.
76. Milgram NW, Head E, Zicker SC, Ikeda-Douglas CJ, Murphey H, Muggenburg B, Siwak C, Tapp D, Cotman CW (2005) Learning ability in aged beagle dogs is preserved by behavioral enrichment and dietary fortification: a two-year longitudinal study. Neurobiol Aging 26, 77-90. (Pubitemid 39600593)
77. Cotman CW, Head E (2008) The canine (dog) model ofhuman aging and disease: dietary, environmental and immunotherapy approaches. J Alzheimers Dis 15, 685-707.
78. Pop V, Head E, Hill MA, Gillen D, Berchtold NC, Muggenburg BA, Milgram NW, Murphy MP, Cotman CW (2010) Synergistic effects of long-term antioxidant diet and behavioral enrichment on beta-amyloid load and non-amyloidogenic processing in aged canines. J Neurosci 30, 9831-9830.
79. Radman T, Parra L, Bikson M (2006) Amplification of small electric fields by neurons; implications for spike timing. Conf Proc IEEE Eng Med Biol Soc 2006, 9831-9839.
80. Fritsch B, Reis J, Martinowich K, Schambra HM, Ji Y, Cohen LG, Lu B (2010) Direct current stimulation promotes BDNF-dependent synaptic plasticity: potential implications for motor learning. Neuron 6, 198-204.
81. Reis J, Robertson E, Krakauer JW, Rothwell J, Marshall L, Gerloff C, Wassermann E, Pascual-Leone A, Hummel F, Celnik PA, Classen J, Floel A, Ziemann U, Paulus W, Siebner HR, Born J, Cohen LG (2008) Consensus: "Can tDCS and TMS enhance motor learning and memory formation?" Brain Stimul 1, 363-369.
82. Hummel FC, Celnik P, Pascual-Leone A, Fregni F, Byblow WD, Buetefisch CM, Rothwell J, Cohen LG, Gerloff C (2008) Controversy: noninvasive and invasive cortical stimulation show efficacy in treating stroke patients. Brain Stimul 1, 370-382.
83. Rozzini L, Costardi D, Chilovi BV, Franzoni S, Trabucchi M, Padovani A (2007) Efficacy of cognitive rehabilitation in patients with mild cognitive impairment treated with cholinesterase inhibitors. Int J Geriatr Psychiatry 22, 356-360. (Pubitemid 46680847)
84. Kukull WA, Higdon R, Bowen JD, McCormick WC, Teri L, Schellenberg GD, van Belle G, Jolley L, Larson EB (2002) Dementia and Alzheimer disease incidence: a prospective cohort study. Arch Neurol 59, 1737-1746. (Pubitemid 35340484)
85. Plassman BL, Langa KM, Fisher GG, Heeringa SG, Weir DR, Ofstedal MB, Burke JR, Hurd MD, Potter GG, Rodgers WL, Steffens DC, Willis RJ, Wallace RB (2007) Prevalence of dementia in the United States: the aging, demographics, and memory study. Neuroepidemiology 29, 1225-1232.